Heat stress destabilizes symbiotic nutrient cycling in corals

Nils Rädecker, Claudia Pogoreutz, Hagen Gegner, Anny Cardenas, Florian Roth, Jeremy Bougoure, Paul Guagliardo, Christian Wild, Mathieu Pernice, Jean-Baptiste Raina, Anders Meibom, Christian R. Voolstra

Research output: Contribution to journalArticlepeer-review

183 Scopus citations

Abstract

Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral–algal symbiosis have been extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral Stylophora pistillata to heat stress prior to the onset of bleaching to identify processes involved in the breakdown of the coral–algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral–algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general.
Original languageEnglish (US)
Pages (from-to)e2022653118
JournalProceedings of the National Academy of Sciences
Volume118
Issue number5
DOIs
StatePublished - Jan 26 2021

Bibliographical note

KAUST Repository Item: Exported on 2021-01-28
Acknowledgements: We thank Dr. Zenon B. Batang and Dr. Nabeel M. Alikunhi for their continuous support and assistance with aquaria maintenance. Further, Ioannis Georgakakis, Mustafa Altunkaya, Gabriela Perna, and Prof. Matt Kilburn are acknowledged for their help and support with
sample processing and data analysis. N.R., C.P., A.C., M.P., J.-B.R., and C.R.V. were supported by the KAUST competitive research grant URF/1/3400-01-01. C.R.V. also acknowledges funding from KAUST and the German Research Foundation (DFG), grant 433042944. A.M. is supported by Swiss National Science Foundation, grant 200021_179092.

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